An environmentally induced multicellular life cycle of a unicellular cyanobacterium

Understanding the evolutionary transition to multicellularity is a key problem in biology.1-4 Nevertheless, the ecological conditions driving such transitions are not well understood. The first known transition to multicel-lularity occurred 2.5 billion years ago in cyanobacteria,5-7 and today's cyanobacteria are characterized by enormous morphological diversity. They range from unicellular species; unicellular cyanobacteria with packet-like phenotypes, e.g., tetrads; and simple filamentous species to highly differentiated filamentous species.8-10 The cyanobacterium Cyanothece sp. ATCC 51142, an isolate from the intertidal zone of the U.S. Gulf Coast,11 was classified as a unicellular species.12 We report a facultative life cycle of Cyanothece sp. in which multicellular filaments alternate with unicellular stages. In a series of experiments, we identified salinity and population density as environmental factors triggering the phenotypic switch between the two morphologies. Then, we used numerical models to test hypotheses regarding the nature of the environmental cues and the mechanisms underlying filament dissolution. While the results predict that the observed response is likely caused by an excreted compound in the medium, we cannot fully exclude changes in nutrient availability (as in Tuomi et al.13 and Matz and Ju center dot rgens14). The best-fit modeling results show a nonlinear effect of the compound, which is characteristic of density-dependent sensing systems.15,16 Furthermore, filament fragmentation is predicted to occur by connection cleavage rather than cell death of each alternating cell, which is supported by fluorescent and scanning electron microscopy results. The switch between unicellular and multicellular morphology constitutes an environmentally dependent life cycle that is likely an important step en route to permanent multicellularity.

Automated summary

Understanding the transition to multicellularity is of great interest in biology, but the ecological conditions driving such transitions are not well understood. In this study, a unicellular species of cyanobacteria, Cyanothece sp. ATCC 51142, was found to exhibit a facultative life cycle with alternating unicellular and multicellular filaments. The switch between these morphologies was triggered by environmental factors such as salinity and population density, indicating the importance of environmental cues in determining the life cycle.